Neural mechanisms underlying the clasp-knife reflex in the cat. II. Stretch-sensitive muscular-free nerve endings

1. The goal of this study was to determine the contribution of muscular free nerve endings to the clasp-knife reflex by comparing their response properties and reflex actions to the clasp-knife reflex. 2. The responses of single muscle afferents were examined in anesthetized cats using stretch and isometric contraction of ankle extensor muscles identical to those that evoked clasp-knife inhibition in decerebrated and dorsal spinal-hemisectioned cats. 3. Fifty-three stretch-sensitive mechanoreceptor afferents were identified as free nerve ending afferents based on their conduction velocities, location within the muscle, uniformity of response, and dissimilarity to other muscle proprioceptors. The afferent conduction velocities were in both the group III (56%) and group II (44%) range, including five fast-conducting group II afferents (> 55 m/s). 4. The stretch response of stretch-sensitive, free nerve endings (SSFNEs) showed several characteristic features: 1) afferents were excited only by large stretches that produced significant passive force; 2) afferent activity began after a brief delay and exhibited segmentation of discharge during ramp stretch, a maximum at the end of ramp stretch, and rapid and complete decay during static stretch, and 3) afferent response adapted to repeated stretches. These properties match those of clasp-knife inhibition described in the companion paper, except that the SSFNE segmentation and maximum were more pronounced and their decay during maintained stretch was more rapid. 5. Isometric contraction produced by electrical stimulation of the muscle nerve, which induced force-evoked inhibition in decerebrated and dorsal hemisectioned cats, also consistently excited SSFNEs. Stretch evoked greater excitation than contraction, indicating that both length and force contribute to SSFNE activity. 6. Stimulation of free nerve endings by squeezing the achilles tendon in cats exhibiting the clasp-knife reflex evoked powerful, homonymous inhibition and a flexion-withdrawal pattern of reflex action - that is, inhibition of extensor and excitation of flexor muscles throughout the hindlimb, which parallels the spatial divergence of the clasp-knife reflex. 7. Intrathecal application of capsaicin, which preferentially blocks the reflex actions of small afferent fibers, blocked clasp-knife inhibition in decerebrated, dorsal hemisectioned cats. 8. The similarities between the reflex actions and response properties of SSFNEs and the properties of the clasp-knife reflex suggest that SSFNEs mediate clasp-knife inhibition. The differences between the responses of SSFNEs and clasp-knife inhibition to stretch and contraction might be explained by spinal 'low-pass' filtering, which may be accomplished by spinal interneurons. Thus the activity of SSFNEs in muscle and tendon appears sufficient to account for the features of the clasp-knife reflex, although additional contributions from Golgi tendon organs and secondary spindle afferents cannot be excluded.